Nematode infections induce distinct chemical signatures and provoke aggression in ants

Nematode infections induce distinct chemical signatures and provoke aggression in ants | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results Nematode infections induce distinct chemical signatures and provoke aggression in ants View ORCID Profile Bhoomika Ashok Bhat , View ORCID Profile Nan-Ji Jiang , View ORCID Profile Rayko Halitschke , View ORCID Profile Yuko Ulrich doi: https://doi.org/10.1101/2025.11.05.686619 Bhoomika Ashok Bhat 1 Lise Meitner Research Group Social Behaviour, Max Planck Institute for Chemical Ecology , Jena, Germany 2 Faculty of Biological Sciences, Friedrich Schiller University Jena , Jena 07743, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Bhoomika Ashok Bhat Nan-Ji Jiang 3 Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology , Jena, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Nan-Ji Jiang Rayko Halitschke 4 Mass Spectrometry and Metabolomics, Max Planck Institute for Chemical Ecology , Jena, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Rayko Halitschke Yuko Ulrich 1 Lise Meitner Research Group Social Behaviour, Max Planck Institute for Chemical Ecology , Jena, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Yuko Ulrich For correspondence: yulrich{at}ice.mpg.de Abstract Full Text Info/History Metrics Supplementary material Preview PDF Abstract Maintaining group integrity by excluding outsiders and pathogens is a fundamental requirement and challenge of social living. In social insects, these defences rely heavily on chemical communication, with cuticular hydrocarbons (CHCs) mediating both nestmate recognition and infection-related social responses. In ants, CHCs are stored and homogenised in the pharyngeal gland, contributing to the formation of a shared colony odour that enables nestmate recognition. We investigated the behavioural and chemical responses of the clonal raider ant Ooceraea biroi to infections by the nematode Diploscapter sp ., which specifically infects the pharyngeal gland. Using behavioural and chemical analyses, we show that: 1) infected ants elicit increased aggression from uninfected nestmates and non-nestmates, consistent with a social immune defence that limits parasite entry in colonies, 2) aggression is likely driven by infection-specific changes in CHC profiles, and 3) infections do not compromise nestmate recognition, which acts through distinct CHCs. Thus, while many parasitic nematodes can evade host immune recognition, Diploscapter fails to evade the social recognition system of its host. The efficient detection and exclusion of infected individuals likely reduce parasite introduction and transmission both within and between colonies. Introduction Group living offers major benefits but also poses a fundamental challenge: maintaining the integrity of the social group by preventing the entry and spread of “non-self” organisms, including both intruders and parasites. Across the animal kingdom, social species discriminate between group members and outsiders [ 1 ] using olfactory [ 2 – 4 ], visual [ 5 , 6 ], or acoustic [ 7 ] cues. In many systems, individuals can also discriminate between healthy and infected social partners using the same sensory modalities [ 8 – 11 ]. While outsiders generally elicit antagonistic behaviour like aggression or avoidance, infected group members can trigger social behaviours ranging from affiliative behaviours like care or grooming [ 12 , 13 ] to antagonistic behaviour like avoidance or aggression [ 10 , 14 , 15 ]. As supremely social organisms, social insects have evolved efficient mechanisms to maintain colony integrity by defending against both outsiders and disease. Colonies typically respond with aggression toward non-nestmates [ 2 ] while responses to infected nestmates are remarkably flexible, ranging from care [ 16 – 20 ] to exclusion or cannibalisation [ 16 , 21 , 22 ], depending on the pathogen [ 16 ] or the stage of infection [ 20 , 22 ]. Despite the sophistication of these collective defences, detection of both non-nestmates and infected nestmates is imperfect, and some (social) parasites can evade recognition [ 23 – 26 ]. Chemical communication plays a central role in both nestmate recognition and infection-related social responses, and the same class of chemical cues, cuticular hydrocarbons (CHCs), has been implicated in both processes [ 27 ]. CHCs are synthesised by oenocytes in the epidermis and transported to the cuticular surface, where they are exchanged among nestmates through social contact [ 28 ]. In ants, CHCs from different colony members are also stored and mixed in the pharyngeal gland (PG) to generate a shared colony odour [ 29 , 30 ]. This colony odour serves as a template for nestmate recognition, enabling workers to tolerate individuals whose CHC profiles match the template and to attack those that deviate from it [ 31 – 33 ]. Parasite-induced changes in CHC profiles are common [ 27 , 34 – 37 ] and can alter social responses towards infected individuals [ 35 ]. However, most studies compare infected and uninfected individuals without considering nestmate status, leaving it unclear whether the CHC cues used to detect infection overlap with, or are distinct from, the CHC cues used for nestmate recognition. Here, we investigate host chemical and social responses to a nematode parasite ( Diploscapter sp.) that specifically infects the PG of ants ( Fig. 1a ). Our previous work in the clonal raider ant Ooceraea biroi established that Diploscapter infections alter host CHC profiles [ 38 ], indicating that the presence of nematodes in the PG affects cuticular chemistry. Because CHCs mediate both nestmate recognition and infection-related social responses in ants, such alterations may have dual consequences. On one hand, infection-induced changes in CHCs could render infected individuals detectable to nestmates. On the other hand, by infecting a gland involved in generating a shared colony odour, nematodes may disrupt the colony’s nestmate recognition system. This possibility is consistent with the general ability of parasitic nematodes to evade host immune recognition [ 23 ], raising the question of whether they can also evade host social recognition systems. We therefore ask whether Diploscapter infections (i) can be detected by social partners and induce behavioural responses and/or (ii) impair the discrimination between nestmates and non-nestmates. Download figure Open in new tab Figure 1: Infected ants receive increased aggression. a) Micro-CT reconstruction showing Diploscapter nematodes (red) in the pharyngeal gland (purple) of a clonal raider ant. Scale bar: 0.1 mm. Image adapted from [ 38 ]. b) Experimental design. Focal ants that were either infected (red) or uninfected (blue) and either nestmates (light colours) or non-nestmates (dark colours) were introduced in uninfected colonies to measure behavioural responses, or used in chemical analyses. c) Ethograms showing antennation (events; purple) and biting (duration; yellow) in two representative colonies exposed to an uninfected nestmate (top) and an infected non-nestmate (bottom). Each row represents the behaviour of one ant towards the focal individual. d) Normalised antennation received by infected (red) and uninfected (blue) ants that were either nestmates (light colours, squares) or non-nestmates (dark colours, triangles). Boxplots: thick bars indicate the median, boxes indicate the interquartile range (IQR), whiskers represent 1.5 times the IQR (maxima: Q3 + 1.5 * IQR, minima: Q1 − 1.5 * IQR). Shaded areas are kernel density estimates truncated at the minimum and maximum data values. Data points represent focal individuals. e) Normalised biting received by infected (red) and uninfected (blue) focal ants that were either nestmates (light colours, squares) or non-nestmates (dark colours, triangles). Values can exceed 1 if focal ants were bitten by multiple ants simultaneously. Boxplots, data points, and shaded area as in (d). We address these questions in O. biroi , a queenless species in which colonies are composed of genetically identical workers that reproduce asexually and synchronously [ 39 – 41 ]. Workers are aggressive towards non-nestmates, especially individuals from different asexual lineages [ 42 ]. To test whether Diploscapter infection interferes with this recognition system, we quantified behavioural responses of uninfected colonies toward infected and uninfected nestmates and non-nestmates and analysed CHC profiles to identify the chemical basis of these responses. Materials and Methods Nematodes Diploscapter nematodes infect the PG of ants at the developmentally arrested ‘dauer’ larval stage [ 38 ]. To produce dauer larvae, eggs and gravid adults from 2–3 60 mm Nematode Growth Medium (NGM) agar plates were washed in 3 mL of ddH 2 O, centrifuged for 1 min at 56 g, and the resulting pellet was resuspended in 1 mL of ddH 2 O. The nematode suspension was treated with a bleach solution (3 mL 5% NaClO + 1 mL 1 M NaOH) and vortexed for 4 min to kill larvae and adults, and obtain a solution of eggs, as in [ 38 ]. The egg suspension was washed twice in ddH 2 O and centrifuged at 56 g for 1 min to obtain a pellet, which was resuspended in 300 µL of ddH 2 O and transferred to cholesterol-depleted NGM-agar plates seeded with 20 µL of E. coli OP50 to promote dauer formation [ 43 ]. After hatching overnight into L1 larvae at 28 °C, larvae were transferred to 1.5 g of cholesterol-depleted NGM-agar to develop into infective dauers. Infecting ants Diploscapter infects adult ants but not the brood [ 38 ]. To obtain nematode-free ants, pupae nearing eclosion were collected from stock colonies and allowed to eclose in sterilised nest boxes. One day post-eclosion, the resulting workers were surface sterilised in 1% NaClO and transferred to new sterilised nest boxes. This procedure was repeated the next day. When they were 10 days old, workers were divided into infected (80–200 ants) and uninfected (2 groups of 200–400 ants each) groups. For infected groups, 1.5 g of cholesterol-depleted NGM-agar seeded with 100 µL of a Diploscapter L1 larvae inoculum (at a concentration corresponding to 200–300 nematodes/ant) was introduced. L1 larvae developed into dauers and infected the ants [ 38 ]. Infections were monitored regularly by dissecting 3–5 workers. When infection loads reached ca. 30 nematodes/ant, infections were terminated by transferring ants to nematode-free nest boxes. Infection loads in field-collected ants can reach 85 nematodes/ant [ 44 ], so the experimental loads used here were ecologically realistic. For uninfected groups, 1.5 g of nematode-free cholesterol-depleted NGM-agar was introduced. Ants were fed sterilised Tetramorium bicarinatum brood five times weekly. Nestmate recognition experiments Nestmate recognition experiments were repeated thrice using the same basic design (Supplementary table S1): ten uninfected “social environment” ants were exposed to one focal ant that was either infected or uninfected, and either a nestmate or a non-nestmate, forming four treatment groups. Nestmates were ants from the same clonal lineage, whereas non-nestmates were of a different lineage (Supplementary table S1). In Experiments 1 and 2, both social environment ants and focal ants were from lineages A or B and B or D, respectively [ 45 ]. In Experiment 3, all social environment ants were from lineage B, and focal ants were from lineages A, B, or D. Irrespective of treatment, focal and social environment ants were sampled from different boxes and had therefore been physically separated for the same amount of time before the experiment, ensuring that behavioural responses were not confounded by housing conditions. All social environment ants were paint-marked (UniPaint PX-20) on the gaster and thorax to be individually recognised in video analyses. Two days after paint-marking, they were split into experimental colonies of ten ants each, placed in one chamber of custom two-chamber arenas (15 mm long × 12 mm wide × 5 mm high; laser-cut acrylic with). After ca. 15h of acclimation, one unmarked focal ant was added to the second chamber (4 × 12 × 5 mm) of each arena, and the separation between the two chambers was removed, allowing focal and social environment ants to interact. Videos were recorded for 24 h at 20 frames per second using 6 Basler (model acA20440-20gc; Ahrensburg, Germany) cameras and the LoopBio Motif (v.6) software. Focal ants that died during the experimental setup were excluded from further analyses. No ants died during the experiment. The behaviour of the social environment ants toward the focal ant was annotated manually using BORIS (v8.1) by one experimenter, blinded to treatment. In each arena, behavioural scoring started at the first contact between any social environment ant and the focal ant and lasted 11, 7, and 5 min in Experiments 1, 2, and 3, respectively, based on our observation that a shorter scoring duration qualitatively recapitulated results obtained from longer scoring. Two discrimination behaviours, antennation and biting, were scored as previously [ 42 ]. Antennation was defined as events where a worker drummed her antennae rapidly on the focal ant’s body. Biting was defined as events when a worker dragged the focal ant with her mouthparts (Supplementary Movie 1). In each arena, the number of antennation events and the duration of biting were summed across all social environment ants and normalised by the duration of behavioural scoring. Thus, the normalised duration of biting could exceed 1 if the focal ant received biting from multiple ants simultaneously. Chemical analyses Chemical analyses were conducted on ants from Experiment 3, which were not used in behavioural assays, to rule out changes in CHC profiles resulting from social interactions (e.g., received aggression), rather than causing them. Seven days after the end of Experiment 3, ten uninfected and infected ants from each of the three clonal lineages (A, B and D) were decapitated, the heads dissected to measure infection loads and the (headless) bodies used for chemical analyses. Each body was immersed in 150 µL n-hexane containing 0.33 ng/µL of 1-bromotetradecane as internal standard (IS) for 15 min. Surface extracts were concentrated to approximately 50 µL under N 2 flow, and 1 µL was injected in the splitless mode at 250 °C into a Shimadzu QP2010 gas chromatograph-mass spectrometry (GC-MS), equipped with a SLB-5MS GC column (30 m × 0.25 mm × 0.25 μm, Supelco, USA) and helium as carrier gas (1.2 mL min −1 ). The temperature was programmed for 3 min at 50 °C, followed by a 10 °C/min ramp to 300 °C and finally for 10 min at 300 °C. Mass spectra were recorded with electron impact ionisation at 70 eV. The software GCMSsolution (v4.20, Shimadzu Corporation) was used for data analysis. CHC compounds were annotated by comparisons of spectra and diagnostic fragmentation pattern with library databases and calculation of retention indices with a co-injected standard n-alkane solution (1 ng/ µL, C 7 -C 30 , 99%, Sigma-Aldrich). Unidentified CHCs were named with their corresponding retention indices (RIs). To calculate the relative abundance of CHC compounds, the area under each CHC peak was integrated (Extracted Ion Chromatogram m/z 57) and divided by the total area under all CHC peaks. Absolute CHC concentrations were calculated from the IS-normalised peak area and the response factors of the n-alkane with the identical carbon chain length. Response factors were calculated from calibration curves using the IS-normalised peak areas of a dilution series of the C 7 –C 30 n-alkane mix (5, 10, 25, 50, 100 ng/µL). To calculate total CHC abundance, the absolute abundance of all CHC was summed. Statistical analyses Statistical analyses were conducted in R v4.5.1 [ 46 ]. The three behavioural experiments were analysed together. The normalised antennation events and duration of biting received by focal ants were modelled using generalised linear mixed models (GLMMs) with a Tweedie distribution and log link function implemented with the function glmmTMB from the package glmmTMB [ 47 ]. Both models included infection status (infected vs. uninfected), nestmate status (nestmate vs. non-nestmate), and their interaction as fixed predictors, and the clonal lineage of the social environment as a random factor. The fixed predictor contributions were evaluated by sequentially deleting terms using drop1 from the stats package [ 48 ].To test whether the lineage of focal ants affected the infection-induced aggression they received, we used a separate GLMM for each lineage, with infection status (infected vs. uninfected) as a fixed predictor and the clonal lineage of the social environment as a random factor. The fixed predictor contributions were evaluated with drop1 followed by Benjamini-Hochberg correction for multiple testing. The total abundance of CHCs was compared using lineage-specific Kruskal-Wallis tests between infected and uninfected ants, with Benjamini-Hochberg correction for multiple testing. The relative abundance of CHCs was visualised with a nonmetric multidimensional scaling (NMDS) analysis using a Bray-Curtis dissimilarity matrix with the metaMDS function from the package vegan [ 49 ]. The effect of infection status (infected vs. uninfected) and clonal lineage (A, B, or D) on CHC profiles was analysed using a permutational multivariate analysis of variance on the Bray-Curtis dissimilarity matrix with the adonis function from the vegan package [ 49 ]. Individual CHCs predicting infection status and clonal lineage were identified with random forest analyses on the CHC relative abundance separately for infection status and clonal lineage using the randomForest function from the randomForest package [ 50 ]. The model accuracy was estimated using the out-of-box error (OOB) rate, which is calculated by aggregating the prediction errors for each sample using only the trees that were not trained on that sample. Accuracy was calculated as (100 – OOB)%. Results To test if nematode infections affect nestmate recognition behaviour, we exposed groups of ten uninfected ants to one focal ant that was either a nestmate or a non-nestmate, and either infected or uninfected ( Fig. 1b ), and measured the attention (antennation) and aggression (biting) received by that focal individual ( Fig. 1c ). Interactions typically started with antennation, which could escalate into biting depending on the focal ant’s identity. The number of responding colony members ranged from 0 to 8, so that focal ants were often simultaneously antennated or bitten by multiple group members ( Fig. 1c , Supplementary Movie 1). As expected, non-nestmates received more antennation (GLMM, nestmate status: df = 1, LRT = 51.316, p = 7.864 × 10 -13 ) and biting (df = 1, LRT = 49.469, p = 2.015 × 10 -12 ) than nestmates, confirming that clonal raider ants discriminate non-nestmates, even when kept under standardised laboratory conditions. Contrary to our expectations, nematode infections did not affect the ability of ants to distinguish nestmates and non-nestmates. Instead, infected ants received more antennation (GLMM, infection status: df = 1, LRT = 24.770, p = 6.459 × 10 -7 ) and biting (df = 1, LRT = 13.101, p = 2.951 × 10 -4 ) than their uninfected counterparts, independent of their nestmate status. Nestmate status and infection status increased attention and aggression in an additive manner (GLMM, nestmate status × infection status: antennation: df = 1, LRT = 0.801, p = 0.371; biting: df =1, LRT = 3.812, p = 0.051), so that infected non-nestmates received the highest amount of aggression ( Fig. 1e ). Thus, clonal raider ants detect and attack nematode-infected workers. We asked whether this effect might arise through a passive physical process. Infecting nematodes can occupy a large fraction of the PG ( Fig. 1a ), reducing the space available for glandular contents such as CHCs. CHCs that would normally enter the PG may instead remain on the cuticle, leading to an overall increase in their abundance. Such an increase could, in turn, accentuate existing differences in CHC profiles among individuals, thereby enhancing recognition and aggression toward infected ants. To quantify CHC abundance, we washed the body surface of infected and uninfected ants from three clonal lineages (A, B, and D) in hexane ( Fig. 1b ) and analysed these washes using GC-MS. Infections increased the total CHC abundance in only one lineage ( Fig. 2a ; Kruskal-Wallis tests, lineage A: adjusted p = 0.81, lineage B: p = 0.82, lineage D: p = 0.002). However, infection only increased aggression in the other two lineages (GLMM, infection status: lineage A: df = 1, LRT = 7.554, adjusted p = 0.017; lineage B: df = 1, LRT = 4.659, p = 0.046; lineage D: df = 1, LRT = 1.229, p = 0.268). Therefore, it is unlikely that increased aggression was driven by increased total CHC abundance. Thus, we next asked whether nematode infections modified the relative abundance of CHCs. Download figure Open in new tab Figure 2: Chemical signatures of infection are distinct from nestmate recognition cues. a) Total abundance of all CHCs in infected (red) and uninfected (blue) ants. Thick bars indicate the median, and the box indicates the IQR around the median, and whiskers represent 1.5 times the IQR (maxima: Q3 + 1.5 * IQR, minima: Q1 − 1.5 * IQR). Shaded areas are kernel density estimates truncated at the minimum and maximum data values. Data points represent (decapitated) individuals. b) CHC profiles of infected (red, open symbols) and uninfected (blue, solid symbols) ants from lineages A (squares), B (triangles) and D (circles), visualised with an NMDS analysis. Data points represent (decapitated) individuals. c) Relative importance of 17 CHCs as predictors of infection status (green) and lineage (purple). **: p<0.01. As reported previously [ 19 , 38 , 51 ], clonal lineages differed in CHC composition (Adonis: lineage: R 2 = 0.284, F = 12.252, p = 0.001) and infections altered CHC profiles (Adonis: infection status: R 2 = 0.066, F = 5.714, p = 0.006). Therefore, infection-mediated changes in CHC relative abundance, but not total abundance, correlated with behavioural responses towards infected individuals. We then tested whether putative infection cues overlap with nestmate recognition cues, using random forest models to identify CHCs that best predicted infection status (model prediction accuracy: 91.7%) and clonal lineage (model prediction accuracy: 96.7%). The top four predictors of infection status (each contributing more than a 50% decrease in model prediction accuracy) (Supplementary table S3) did not overlap with the top four predictors of clonal lineage ( Fig. 2c ), indicating that the chemical signatures of infection status and of clonal lineage were driven by different CHCs. Hence, host CHC profiles undergo infection-specific changes that are largely distinct from nestmate recognition cues. Discussion Ants infected with Diploscapter nematodes received markedly elevated aggression from both uninfected nestmates and non-nestmates. In natural settings, infected individuals that encounter aggression at the nest entrance would likely retreat, consistent with a social immune defence that limits parasite entry in colonies. Reports of social immune responses to nematode-infected nestmates in social insects are rare [ 52 , 53 ], with most work focusing on other taxa, such as entomopathogenic fungi [ 17 , 19 , 21 , 22 , 54 ] and viruses [ 18 , 34 , 55 ]. Parasitic nematodes are known for evading host immune recognition [ 23 , 56 ]. The detection and attack of infected ants observed here indicates that Diploscapter fails to escape its host’s social recognition system, underscoring the efficiency with which ants defend their colonies from parasites. Aggressive responses to infected nestmates are exceedingly rare in ants, with, to our knowledge, the only reports involving brood rather than adults [ 21 , 57 ]. By contrast, much of the literature documents caregiving responses towards exposed or infected adult ants, often in the form of grooming of fungal spores from the cuticle [ 16 , 58 , 59 ], which effectively controls the infection. In the present system, where nematodes infect an internal organ, grooming would likely fail to mitigate infection, and preventing entry of parasitised individuals might be the more effective colony-level defence strategy. Our chemical analyses indicate that these behavioural effects are associated with infection-specific shifts in CHC composition, which may render infection status perceivable to other ants. The mechanistic basis of these shifts remains unresolved. They could, in principle, be parasite-mediated if nematodes modify CHCs within the PG, for example, by consumption or alteration, before they are transferred to the cuticle through grooming. Alternatively, changes in CHC profiles could be host-mediated if infections trigger physiological or immune processes that modulate CHC biosynthesis. Our previous work showed that Diploscapter infection alters host gene expression in the PG, including immune-related genes [ 38 ], and immune-triggered CHC changes have been reported in other social insects [ 34 – 36 , 60 ]. Both mechanisms are therefore plausible and possibly concurrent. However, whether infection-induced CHC changes cause aggression, or merely correlate with it, remains to be determined. These findings complement our earlier work on the same host–parasite system [ 38 ], which examined colony-level effects of infection over longer timescales, and found spatial organisation patterns that appeared to favour parasite transmission. Several methodological and biological differences likely account for the different behavioural patterns observed. Infection loads in the earlier study were approximately threefold lower (mean ± SD: 10.00 ± 4.16 nematodes/ant in [ 38 ] vs. 36.39 ± 22.73 nematodes/ant here), which may have rendered infections more difficult to detect by other ants. In addition, here we measured immediate behavioural responses within minutes of encounter, whereas the previous study focused on spatial behaviour aggregated over several days, possibly masking any early aggressive interactions. Clonal raider ants of different lineages readily form mixed colonies under laboratory conditions [ 61 ], suggesting that initial aggression does not preclude eventual tolerance or cohabitation. The two studies may therefore capture behavioural consequences of infection unfolding at distinct phases of host–parasite interaction, from initial recognition to longer-term adjustment. Combining behavioural and chemical profiling, our study shows that ant colonies can efficiently detect and reject infected conspecifics. Our results extend comparable findings in other taxa, from honey bees showing aggression towards virus- and mite-infested individuals [ 33 , 60 ] to primates where sick individuals are more likely to receive aggression from group mates [ 62 ], and show that internal infections with nematodes, arguably more cryptic than the fungal spores commonly used in social insect research, can also elicit social immune responses. Functionally, detection and exclusion of infected individuals at the nest boundary should reduce parasite introduction and transmission both within and between colonies, potentially constituting an important defence mechanism in social insects. Author contributions B.A.B.: conceptualization, methodology, data acquisition, data curation, data analysis, visualization, writing - original draft, writing - review and editing; N.J.J.: initial chemical analysis setup, writing - review and editing; R.H.: chemical methodology, analysis, supervision, writing - review and editing; Y.U: conceptualisation, funding acquisition, methodology, visualisation, project administration, resources, supervision, validation, writing - original draft, writing - review and editing. All authors contributed, reviewed and approved the manuscript for publication. Conflict of interest The authors declare no conflict of interest. Acknowledgements The authors thank Daniel Veit for help with arena design and production, Erik Frank, Markus Knaden, and Patrizia d’Ettorre for input on experimental design, Tim Zetzsche for assistance in ant dissection, and all the members of the Social Behaviour group, as well as Ebi Antony George for discussions. This is Clonal Raider Ant Project paper no. 44. References 1. ↵ Gokcekus S , Firth JA , Regan C , Sheldon BC . 2021 Recognising the key role of individual recognition in social networks . Trends Ecol. Evol . 36 , 1024 – 1035 . ( doi: 10.1016/j.tree.2021.06.009 ) OpenUrl CrossRef 2. ↵ van Zweden JS , d’Ettorre P. 2010 Nestmate recognition in social insects and the role of hydrocarbons . Insect Hydrocarb. Biol. Biochem. Chem. Ecol . 11 , 222 – 243 . OpenUrl 3. Johnston RE . 2003 Chemical Communication in Rodents: from Pheromones to Individual Recognition . J. Mammal . 84 , 1141 – 1162 . ( doi: 10.1644/BLe-010 ) OpenUrl CrossRef 4. ↵ Thom MD , Hurst JL . 2004 Individual recognition by scent . Ann. Zool. Fenn . 41 , 765 – 787 . OpenUrl Web of Science 5. ↵ Tibbetts EA , Pardo-Sanchez J , Ramirez-Matias J , Avarguès-Weber A. 2021 Individual recognition is associated with holistic face processing in Polistes paper wasps in a species-specific way . Proc. R. Soc. B Biol. Sci . 288 , 20203010 . ( doi: 10.1098/rspb.2020.3010 ) OpenUrl CrossRef PubMed 6. ↵ Morita T , Toyoda A , Aisu S , Kaneko A , Suda-Hashimoto N , Matsuda I , Koda H. 2020 Animals exhibit consistent individual differences in their movement: A case study on location trajectories of Japanese macaques . Ecol. Inform . 56 , 101057 . ( doi: 10.1016/j.ecoinf.2020.101057 ) OpenUrl CrossRef 7. ↵ Chuang M-F , Kam Y-C , Bee MA . 2017 Territorial olive frogs display lower aggression towards neighbours than strangers based on individual vocal signatures . Anim. Behav . 123 , 217 – 228 . ( doi: 10.1016/j.anbehav.2016.11.001 ) OpenUrl CrossRef 8. ↵ Ghai RR , Fugère V , Chapman CA , Goldberg TL , Davies TJ . 2015 Sickness behaviour associated with non-lethal infections in wild primates . Proc. R. Soc. B Biol. Sci . 282 , 20151436 . ( doi: 10.1098/rspb.2015.1436 ) OpenUrl CrossRef PubMed 9. Butler MJ IV , Behringer DC . 2021 Behavioral Immunity and Social Distancing in the Wild: The Same as in Humans? BioScience 71 , 571 – 580 . ( doi: 10.1093/biosci/biaa176 ) OpenUrl CrossRef 10. ↵ Poirotte C , Massol F , Herbert A , Willaume E , Bomo PM , Kappeler PM , Charpentier MJE . 2017 Mandrills use olfaction to socially avoid parasitized conspecifics . Sci. Adv . 3 , e1601721 . ( doi: 10.1126/sciadv.1601721 ) OpenUrl FREE Full Text 11. ↵ Côté A , Binning SA . 2025 Importance of visual and chemical cues in infection detection and avoidance in freshwater fish . Anim. Behav . 222 , 123060 . ( doi: 10.1016/j.anbehav.2024.123060 ) OpenUrl CrossRef 12. ↵ Rasa , O. A. E. 1976 . Invalid care in the dwarf mongoose (Helogale undulata rufula) . Zeitschrift für Tierpsychologie 42 , 337 – 349 . ( doi: 10.1111/j.1439-0310.1976.tb00975.x ) OpenUrl CrossRef 13. ↵ Schmid-Hempel P. 2017 Parasites and Their Social Hosts . Trends Parasitol . 33 , 453 – 462 . ( doi: 10.1016/j.pt.2017.01.003 ) OpenUrl CrossRef 14. ↵ Arakawa H , Cruz S , Deak T. 2011 From models to mechanisms: Odorant communication as a key determinant of social behavior in rodents during illness-associated states . Neurosci. Biobehav. Rev . 35 , 1916 – 1928 . ( doi: 10.1016/j.neubiorev.2011.03.007 ) OpenUrl CrossRef PubMed 15. ↵ Behringer DC , Butler MJ , Shields JD . 2006 Avoidance of disease by social lobsters . Nature 441 , 421 – 421 . ( doi: 10.1038/441421a ) OpenUrl CrossRef PubMed Web of Science 16. ↵ Cremer S , Armitage SAO , Schmid-Hempel P. 2007 Social Immunity . Curr. Biol . 17 , R693 – R702 . ( doi: 10.1016/j.cub.2007.06.008 ) OpenUrl CrossRef PubMed Web of Science 17. ↵ Tragust S , Mitteregger B , Barone V , Konrad M , Ugelvig LV , Cremer S. 2013 Ants Disinfect Fungus-Exposed Brood by Oral Uptake and Spread of Their Poison . Curr. Biol . 23 , 76 – 82 . ( doi: 10.1016/j.cub.2012.11.034 ) OpenUrl CrossRef PubMed 18. ↵ Baracchi D , Fadda A , Turillazzi S. 2012 Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies . J. Insect Physiol . 58 , 1589 – 1596 . ( doi: 10.1016/j.jinsphys.2012.09.014 ) OpenUrl CrossRef PubMed 19. ↵ Alciatore G , Ugelvig LV , Frank E , Bidaux J , Gal A , Schmitt T , Kronauer DJC , Ulrich Y. 2021 Immune challenges increase network centrality in a queenless ant . Proc. R. Soc. B Biol. Sci . 288 , 20211456 . ( doi: 10.1098/rspb.2021.1456 ) OpenUrl CrossRef PubMed 20. ↵ Cremer S , Pull CD , Fürst MA . 2018 Social Immunity: Emergence and Evolution of Colony-Level Disease Protection . Annu. Rev. Entomol . 63 , 105 – 123 . ( doi: 10.1146/annurev-ento-020117-043110 ) OpenUrl CrossRef PubMed 21. ↵ Pull CD , Ugelvig LV , Wiesenhofer F , Grasse AV , Tragust S , Schmitt T , Brown MJ , Cremer S. 2018 Destructive disinfection of infected brood prevents systemic disease spread in ant colonies . eLife 7 , e32073 . ( doi: 10.7554/eLife.32073 ) OpenUrl CrossRef PubMed 22. ↵ Davis HE , Meconcelli S , Radek R , McMahon DP . 2018 Termites shape their collective behavioural response based on stage of infection . Sci. Rep . 8 , 14433 . ( doi: 10.1038/s41598-018-32721-7 ) OpenUrl CrossRef PubMed 23. ↵ Castillo JC , Reynolds SE , Eleftherianos I. 2011 Insect immune responses to nematode parasites . Trends Parasitol . 27 , 537 – 547 . ( doi: 10.1016/j.pt.2011.09.001 ) OpenUrl CrossRef PubMed Web of Science 24. Powell S , Del-Claro K , Feitosa RM , Brandão CRF. 2014 Mimicry and Eavesdropping Enable a New Form of Social Parasitism in Ants . Am. Nat . 184 , 500 – 509 . ( doi: 10.1086/677927 ) OpenUrl CrossRef PubMed 25. Van Oystaeyen A , Araujo Alves D , Caliari Oliveira R , Lima do Nascimento D , Santos do Nascimento F , Billen J , Wenseleers T. 2013 Sneaky queens in Melipona bees selectively detect and infiltrate queenless colonies . Anim. Behav . 86 , 603 – 609 . ( doi: 10.1016/j.anbehav.2013.07.001 ) OpenUrl CrossRef 26. ↵ Lenoir A , D’Ettorre P , Errard C , Hefetz A. 2001 Chemical Ecology and Social Parasitism in Ants . Annu. Rev. Entomol . 46 , 573 – 599 . ( doi: 10.1146/annurev.ento.46.1.573 ) OpenUrl CrossRef PubMed Web of Science 27. ↵ Sprenger PP , Menzel F. 2020 . Cuticular hydrocarbons in ants (Hymenoptera: Formicidae) and other insects: how and why they differ among individuals, colonies, and species . Myrmecol. News 30 . ( doi: 10.25849/myrmecol.news_030:001 ) OpenUrl CrossRef 28. ↵ Schal C , Sevala VL , Young HP , Bachmann JAS . 1998 Sites of Synthesis and Transport Pathways of Insect Hydrocarbons: Cuticle and Ovary as Target Tissues . Am. Zool . 38 , 382 – 393 . ( doi: 10.1093/icb/38.2.382 ) OpenUrl CrossRef 29. ↵ Soroker V , Vienne C , Hefetz A , Nowbahari E. 1994 The Postpharyngeal Gland as a ‘Gestalt’ Organ for Nestmate Recognition in the Ant Cataglyphis niger . 30. ↵ Crozier RH , Dix MW . 1979 Analysis of two genetic models for the innate components of colony odor in social Hymenoptera . Behav. Ecol. Sociobiol . 4 , 217 – 224 . ( doi: 10.1007/BF00297645 ) OpenUrl CrossRef Web of Science 31. ↵ Lahav S , Soroker V , Hefetz A , Vander Meer RK . 1999 Direct Behavioral Evidence for Hydrocarbons as Ant Recognition Discriminators . Naturwissenschaften 86 , 246 – 249 . ( doi: 10.1007/s001140050609 ) OpenUrl CrossRef Web of Science 32. Blomquist GJ , Bagnères A-G. 2010 Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology . Cambridge University Press . 33. ↵ d’Ettorre P , Lenoir A. 2010 Nestmate recognition . Ant Ecol ., 194 – 209 . 34. ↵ Geffre AC et al. 2020 Honey bee virus causes context-dependent changes in host social behavior . Proc. Natl. Acad. Sci . 117 , 10406 – 10413 . ( doi: 10.1073/pnas.2002268117 ) OpenUrl Abstract / FREE Full Text 35. ↵ Csata E , Casacci LP , Ruther J , Bernadou A , Heinze J , Markó B. 2023 Non-lethal fungal infection could reduce aggression towards strangers in ants . Commun. Biol . 6 , 183 . ( doi: 10.1038/s42003-023-04541-7 ) OpenUrl CrossRef PubMed 36. ↵ Esparza-Mora MA et al. 2023 Defensive behavior is linked to altered surface chemistry following infection in a termite society . Sci. Rep . 13 , 20606 . ( doi: 10.1038/s41598-023-42947-9 ) OpenUrl CrossRef PubMed 37. ↵ De Fazi L , Cervo R , Baracchi D , Bruschini C , Cappa F. 2025 . Biopesticide exposure increases aggression without impairing nestmate recognition in a social paper wasp . Environ. Toxicol . 40 , 1321 – 1331 . ( doi: 10.1002/tox.24547 ) OpenUrl CrossRef PubMed 38. ↵ Li Z et al. 2023 Behavioural individuality determines infection risk in clonal ant colonies . Nat. Commun . 14 , 5233 . ( doi: 10.1038/s41467-023-40983-7 ) OpenUrl CrossRef PubMed 39. ↵ Ravary F , Jaisson P. 2002 The reproductive cycle of thelytokous colonies of Cerapachys biroi Forel (Formicidae, Cerapachyinae) . Insectes Sociaux 49 , 114 – 119 . ( doi: 10.1007/s00040-002-8288-9 ) OpenUrl CrossRef 40. Kronauer DJC , Pierce NE , Keller L. 2012 Asexual reproduction in introduced and native populations of the ant Cerapachys biroi . Mol. Ecol . 21 , 5221 – 5235 . ( doi: 10.1111/mec.12041 ) OpenUrl CrossRef PubMed Web of Science 41. ↵ Oxley PR , Ji L , Fetter-Pruneda I , McKenzie SK , Li C , Hu H , Zhang G , Kronauer DJC . 2014 The Genome of the Clonal Raider Ant Cerapachys biroi . Curr. Biol . 24 , 451 – 458 . ( doi: 10.1016/j.cub.2014.01.018 ) OpenUrl CrossRef PubMed 42. ↵ Kronauer DJC , Tsuji K , Pierce NE , Keller L. 2013 Non–nest mate discrimination and clonal colony structure in the parthenogenetic ant Cerapachys biroi . Behav. Ecol . 24 , 617 – 622 . ( doi: 10.1093/beheco/ars227 ) OpenUrl CrossRef 43. ↵ Matyash V , Entchev EV , Mende F , Wilsch-Bräuninger M , Thiele C , Schmidt AW , Knölker H-J , Ward S , Kurzchalia TV . 2004 Sterol-Derived Hormone(s) Controls Entry into Diapause in Caenorhabditis elegans by Consecutive Activation of DAF-12 and DAF-16 . PLoS Biol . 2 , e280 . ( doi: 10.1371/journal.pbio.0020280 ) OpenUrl CrossRef PubMed 44. ↵ Köhler A. 2012 Nematodes in the heads of ants associated with sap flux and rotten wood . Nematology 14 , 191 – 198 . ( doi: 10.1163/138855411X584142 ) OpenUrl CrossRef 45. ↵ Trible W , McKenzie SK , Kronauer DJC . 2020 Globally invasive populations of the clonal raider ant are derived from Bangladesh . Biol. Lett . 16 , 20200105 . ( doi: 10.1098/rsbl.2020.0105 ) OpenUrl CrossRef PubMed 46. ↵ R Core Team . R: The R Project for Statistical Computing . See https://www.r-project.org/ 47. ↵ Brooks ME et al. 2017 . glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J . 9 ( 2 ): 378 – 400 . OpenUrl 48. ↵ R : The R Stats Package . See https://search.r-project.org/R/refmans/stats/html/00Index.html 49. ↵ Oksanen J , et al. 2025 . vegan: Community Ecology Package. R package version 2. 8-0 . See https://vegandevs.github.io/vegan/ 50. ↵ Liaw A , Wiener M. 2002 . Classification and regression by randomForest . R News 2 ( 3 ): 18 – 22 . See https://CRAN.R-project.org/doc/Rnews/ OpenUrl CrossRef 51. ↵ Teseo S , Lecoutey E , Kronauer DJC , Hefetz A , Lenoir A , Jaisson P , Châline N. 2014 Genetic Distance and Age Affect the Cuticular Chemical Profiles of the Clonal Ant Cerapachys biroi . J. Chem. Ecol . 40 , 429 – 438 . ( doi: 10.1007/s10886-014-0428-y ) OpenUrl CrossRef PubMed 52. ↵ Fujii JK . 1976 Effects of an entomogenous nematode, Neoaplectana carpocapsae Weiser, on the Formosan subterranean termite, Coptotermes formosanus Shiraki, with ecological and biological studies on C. formosanus . 37B , 62 . OpenUrl 53. ↵ Wilson-Rich N , Stuart RJ , Rosengaus RB . 2007 Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae . J. Invertebr. Pathol . 95 , 17 – 25 . ( doi: 10.1016/j.jip.2006.11.004 ) OpenUrl CrossRef PubMed 54. ↵ Rosengaus RB , Maxmen AB , Coates LE , Traniello JFA . 1998 Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae) . Behav. Ecol. Sociobiol . 44 , 125 – 134 . ( doi: 10.1007/s002650050523 ) OpenUrl CrossRef Web of Science 55. ↵ Viljakainen L , Fürst MA , Grasse AV , Jurvansuu J , Oh J , Tolonen L , Eder T , Rattei T , Cremer S. 2023 Antiviral immune response reveals host-specific virus infections in natural ant populations . Front. Microbiol . 14 . ( doi: 10.3389/fmicb.2023.1119002 ) OpenUrl CrossRef 56. ↵ Poinar Jr . G. 2012 Nematode Parasites and Associates of Ants: Past and Present . Psyche J. Entomol . 2012 , 192017 . ( doi: 10.1155/2012/192017 ) OpenUrl CrossRef 57. ↵ Bizzell F , Pull CD . 2024 Ant queens cannibalise infected brood to contain disease spread and recycle nutrients . Curr. Biol . 34 , R848 – R849 . ( doi: 10.1016/j.cub.2024.07.062 ) OpenUrl CrossRef PubMed 58. ↵ Oi DH , Pereira RM . 1993 Ant Behavior and Microbial Pathogens (Hymenoptera: Formicidae) . Fla. Entomol . 76 , 63 – 74 . ( doi: 10.2307/3496014 ) OpenUrl CrossRef 59. ↵ Hughes WOH , Eilenberg J , Boomsma JJ . 2002 Trade-offs in group living: transmission and disease resistance in leaf-cutting ants . Proc. R. Soc. Lond. B Biol. Sci . 269 , 1811 – 1819 . ( doi: 10.1098/rspb.2002.2113 ) OpenUrl CrossRef PubMed Web of Science 60. ↵ Cappa F , Bruschini C , Protti I , Turillazzi S , Cervo R. 2016 Bee guards detect foreign foragers with cuticular chemical profiles altered by phoretic varroa mites . J. Apic. Res . 55 , 268 – 277 . ( doi: 10.1080/00218839.2016.1229886 ) OpenUrl CrossRef 61. ↵ Ulrich Y , Kawakatsu M , Tokita CK , Saragosti J , Chandra V , Tarnita CE , Kronauer DJC . 2021 Response thresholds alone cannot explain empirical patterns of division of labor in social insects . PLOS Biol . 19 , e3001269 . ( doi: 10.1371/journal.pbio.3001269 ) OpenUrl CrossRef PubMed 62. ↵ McFarland R , Henzi SP , Barrett L , Bonnell T , Fuller A , Young C , Hetem RS . 2021 Fevers and the social costs of acute infection in wild vervet monkeys . Proc. Natl. Acad. Sci . 118 , e2107881118 . ( doi: 10.1073/pnas.2107881118 ) OpenUrl Abstract / FREE Full Text View the discussion thread. Back to top Previous Next Posted November 06, 2025. Download PDF Supplementary Material Email Thank you for your interest in spreading the word about bioRxiv. NOTE: Your email address is requested solely to identify you as the sender of this article. Your Email * Your Name * Send To * Enter multiple addresses on separate lines or separate them with commas. 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Share Nematode infections induce distinct chemical signatures and provoke aggression in ants Bhoomika Ashok Bhat , Nan-Ji Jiang , Rayko Halitschke , Yuko Ulrich bioRxiv 2025.11.05.686619; doi: https://doi.org/10.1101/2025.11.05.686619 Share This Article: Copy Citation Tools Nematode infections induce distinct chemical signatures and provoke aggression in ants Bhoomika Ashok Bhat , Nan-Ji Jiang , Rayko Halitschke , Yuko Ulrich bioRxiv 2025.11.05.686619; doi: https://doi.org/10.1101/2025.11.05.686619 Citation Manager Formats BibTeX Bookends EasyBib EndNote (tagged) EndNote 8 (xml) Medlars Mendeley Papers RefWorks Tagged Ref Manager RIS Zotero Tweet Widget Facebook Like Google Plus One Subject Area Animal Behavior and Cognition Subject Areas All Articles Animal Behavior and Cognition (7635) Biochemistry (17690) Bioengineering (13892) Bioinformatics (41936) Biophysics (21451) Cancer Biology (18588) Cell Biology (25499) Clinical Trials (138) Developmental Biology (13378) Ecology (19899) Epidemiology (2067) Evolutionary Biology (24320) Genetics (15609) Genomics (22506) Immunology (17736) Microbiology (40394) Molecular Biology (17181) Neuroscience (88603) Paleontology (666) Pathology (2832) Pharmacology and Toxicology (4824) Physiology (7641) Plant Biology (15152) Scientific Communication and Education (2045) Synthetic Biology (4294) Systems Biology (9825) Zoology (2271)